• Nenhum resultado encontrado

Promoting fruit seedling growth by encapsulated microorganisms

N/A
N/A
Protected

Academic year: 2019

Share "Promoting fruit seedling growth by encapsulated microorganisms"

Copied!
9
0
0

Texto

(1)

1 Corresponding author:

[email protected]

Received: May 15, 2017.

Accepted : October 09, 2017.

Copyright: All the contents of this

journal, except where otherwise noted, is licensed under a Creative Commons Attribution License.

Promoting fruit seedling growth

by encapsulated microorganisms

Carlos Henrique Barbosa Santos

1

, Antonio Baldo Geraldo Martins

2

,

Everlon Cid Rigobelo

2

, Gustavo Henrique de Almeida Teixeira

2

Abstract– The use of microorganisms capable of promoting plant growth has been accepted as an alternative to reducing the use of chemical fertilizers. The aim of this study was to evaluate the inoculation of plant growth promoting microorganisms in seedlings of fruit species, verifying the interaction of the inoculums with encapsulating agents such as clay and alginate. Microbial

inoculums contained the following species: Azospirillum brasilense, Burkolderia cepacia, Bacillus

thuringienses, Bacillus megaterium, Bacillus cereus, Bacillus subtilis, Tricoderma spp. and isolate

411. The fruit species evaluated were: Myrciaria cauliflora (DC.) O. Berg; Myrciaria glazioviana

(Kiaersk.) G. Barros & Sobral; Myrciaria dubia (Kunth) Mc Vaugh; Eugenia brasiliensis Lam.;

Diospyroskaki L.; Garcinia brasiliensis Mart.; Annona muricata L.; Duguetia lanceolata A.

St.-Hil.; Chrysophyllum cainito L.; Anacardium occidentale L.; Eriobotrya japonica (Thunb.) Lindl.

and Litchi chinensis Sonn. The experimental design was completely randomized, in a factorial scheme 3 (control, sodium alginate and clay) x 2 (presence and absence of microbial inoculum) with

five replicates (one seedling per replicate). Seedlings were maintained in 50% of illumination at

an average temperature of 22.5 °C for ninety days, and plant height, diameter, root and shoot dry mass were evaluated. Plant growth promoting microorganisms, regardless of encapsulation used,

promote higher development of C.cainito and L. chinensis seedlings.

Index terms: Fruit plants, development, encapsulation, plant-growth promoting agents.

Promoção do crescimento de mudas frutíferas

por meio de microrganismos encapsulados

Resumo – A utilização de microrganismos capazes de promover o crescimento vegetal tem sido aceita como alternativa à redução do uso de adubos químicos. O objetivo deste trabalho foi avaliar a inoculação de microrganismos promotores do crescimento de plantas em substrato

de mudas de espécies frutíferas, verificando a interação do inóculo com agentes encapsulantes: argila e alginato. O inóculo microbiano continha as seguintes espécies: Azospirillum brasilense, Burkolderia cepacia, Bacillus thuringienses, Bacillus megaterium, Bacillus cereus, Bacillus subtilis, Tricoderma spp. e isolado 411. As espécies frutíferas avaliadas foram: Myrciaria

cauliflora (DC.) O. Berg (jabuticabeira); Myrciaria glazioviana (Kiaersk.) G. Barros & Sobral

(cabeludinha); Myrciaria dubia (Kunth) Mc Vaugh (camu-camu); Eugenia brasiliensis Lam.

(grumixama); Diospyros kaki L. (caqui); Garcinia brasiliensis Mart. (bacupari); Annona

muricata L. (graviola); Duguetia lanceolata A. St. – Hil. (pindaíba); Chrysophyllum cainito

L. (caimito); Anacardium occidentale L. (caju); Eriobotrya japonica (Thunb.) Lindl. (nêspera)

e Litchi chinensis Sonn. (lichia). O delineamento experimental foi o inteiramente casualizado

(DIC), em esquema fatorial 3 (controle, alginato de sódio e argila) x 2 (presença e ausência de inóculo microbiano), com cinco repetições (uma muda por repetição). As mudas foram mantidas em 50% de iluminação, à temperatura média de 22,5 °C, durante noventa dias, sendo avaliados

a altura e o diâmetro do colo das plantas, e a massa seca da parte aérea e das raízes. Micro-organismos promotores de crescimento de plantas, independentemente do encapsulamento utilizado, promovem desenvolvimento superior de mudas de caimito e de lichia.

Termos para indexação: Plantas frutíferas, desenvolvimento, encapsulamento, promotores de crescimento vegetal.

1Agronomist. PhD. in Agronomy (Plant Production). São Paulo State University (UNESP), School of Agricultural and Veterinarian Sciences, Campus of Jaboticabal. Email: [email protected]

(2)

2

C. H. B. Santos et al.

Rev. Bras. Frutic., Jaboticabal, 2018, v. 40, n. 3: (e-179)

Introduction

The production of fruit seedlings is influenced

by abiotic factors, such as light, temperature, gas exchange, water, moisture, substrate and nutrition, and biotic factors, such as pathogens, pests and rhizosphere microorganisms (HARTMANN et al., 2010).

In relation to the substrate, it must be dense and

firm, highly decomposed and stable, sufficiently porous

to drain excess water, free of pests, diseases and weeds, present low salinity, pasteurized or chemically treated, have high cation exchange capacity (CEC), nutrient retention and easy availability (HARTMANN et al., 2010). In addition, biotic factors, such as rhizosphere microorganisms (mycorrhizal bacteria and fungi), can

influence the development of seedlings, and plant growth promoting bacteria (PGPB) exert beneficial effects by stimulating, for example, nitrogen fixation (BEUTLER

et al., 2016), nutrient solubilization (MAJEED et al., 2015), production of plant regulators (FAHAD et al., 2015) and increase of root absorption capacity (PII et al., 2006).

Indirectly, PGPB acts as biological control agents against pathogens present in the substrate, possibly through the production of hydrocyanic acid, bactericides

and antibiotics, by space competition, uptake of Fe+3

and other nutrients, parasitism, resistance induction and cross protection (MOTA et al., 2017).

In relation to PGPB species, the genus

Azospirillum has several species that grow widely in the rhizosphere of grasses and, after being isolated and used in plant production, presented positive responses

on productivity and on biological nitrogen fixation

(BNF) (HUNGRIA et al., 2015; MÜLLER et al., 2016;

PEREG et al., 2016). Burkholderia cepacia is another

important species of bacteria in the BNF process (GÓES

et al., 2015). Bacillus isolates have been shown to have

satisfactory effects when used as biocontrol agents and

to promote plant growth, highlighting Bacillus subtilis

and Bacillus cereus isolates (SOUZA et al., 2017),

Bacillus thuringienses (CONSTANSKI et al., 2015) and Bacillus megaterium (ZHOU et al., 2016). Among

fungi, Trichoderma spp. stands out as a biocontrol agent

(CONTRERAS-CORNEJO et al., 2016) and also in plant growth promotion ((NIETO-JACOBO et al., 2017).

One way of incorporating PGPB into substrates is to encapsulate solid, liquid and gaseous materials into small capsules that release their contents under controlled conditions. Encapsulation is important for maintaining the stability of microorganisms and for increasing the resistance of bacteria in the substrate. Among the many types of encapsulating materials, calcium and sodium alginate, as well as whey proteins and gums have been the most widely used (SCHOEBITZ et al., 2013; VEMMER; PATEL, 2013). Clay is also a good encapsulating agent

with properties different from alginate, but maintaining the desired properties of an encapsulating agent. The use of clay for the preservation of conidia has demonstrated satisfactory effect in storage, guaranteeing the viability of this for a long period (SHI, 1988).

The isolated or combined inoculation of microorganisms may constitute a biotechnological tool of interest in the production of fruit plants. In this context, the aim of this study was to evaluate the effect of inoculation of microorganisms (PGPB) on substrate used for seedlings of fruit species, verifying the interaction of the inoculum with encapsulating agents clay and sodium alginate.

Material And Methods

The experiment was conducted between March

16 and June 16, 2015 (90 days) in the Fruit field of the

School of Agricultural and Veterinarian Sciences, São Paulo State University (UNESP), Campus of Jaboticabal, located in the following geographical coordinates (lat 21º14’05’’S, long 48º17’09’’W, 590 m above sea level). The climate of the region, according to the Köppen

classification is Cwa, with average annual temperature

of 22 ºC.

The inoculum used contained the following species

of microorganisms: Azospirillum brasilense, Burkolderia

cepacia, Bacillus thuringienses, Bacillus megaterium, Bacillus cereus, Bacillus subtilis, Tricoderma spp.

and isolate identified as 411. All microorganisms are

preserved in the collection of the Laboratory of Soil Microbiology of the Department of Plant Production - UNESP, Campus of Jaboticabal.

Microorganisms were separately cultured in flasks

containing nutritive broth for seven days and incubated in B.O.D. oven (Biochemical Oxygen Demand) (Eletrolab, model 347 F, Brazil), at 25 ºC. After the incubation period, microorganisms were separately centrifuged at 10,000 rpm for 10 min at 28°C (Novatecnica, model MLW K24, Brazil). The inoculum concentration was standardized as recommended by Barry and Thornsberry

(1991) and Sahm and Washington II (1991) in 1 x 107

CFU mL-1, using a spectrophotometer (Micronal, model

B382, Brazil) at absorbance at 695 nm.

To each microorganism solution, sodium alginate

solution (NaC6H7O6) at concentration of 1% (w/v) was

added. The microorganism solutions added of sodium alginate were dripped in 0.1M calcium chloride solution

(CaCl2), giving rise to beads with the microbial inoculum

(SHEU; MARSHALL, 1993; SULTANA et al., 2000). Beads were then washed with distilled water using a sieve

and submitted to drying in a laminar flow chamber for a

(3)

applied in each pot, each seedling received 96 microbial beads, which were incorporated into the substrate in a hole at approximately 10 cm in depth in order to guarantee a greater proximity of the material deposited in the substrate with the roots of seedlings. Treatment containing alginate received only sodium alginate beads without the presence of the microbial inoculum, and 96 beads per pot were added.

In order to inoculate microorganisms with clay, suspension was prepared containing 1 mL of each microorganism was prepared for 1 mL of clay in the

dilution of 1: 3 (w/v) distilled water (adapted from

CARNEIRO, GOMES, 1997). Each pot received a total of 8 mL of microbial inoculum added to 8 mL of clay, which were incorporated into the substrate in hole of approximately 10 cm in depth, totaling 16 mL per pot. For treatment containing only clay, the same procedure was performed, excluding only the addition of the microbial inoculum.

All seedlings of fruit species studied were originated from seeds obtained from mother plants belonging to the Germplasm Active Bank of UNESP, Campus de Jaboticabal, conducted in one plant per pot. Microorganisms were inoculated on substrates where seedlings of the following fruit species were

being conducted: Myrciaria cauliflora (DC.) O. Berg

(jabuticaba); Myrciaria glazioviana (Kiaersk.) G. Barros &

Sobral (cabeludinha); Myrciaria dubia (Kunth) Mc Vaugh

(camu-camu); Eugenia brasiliensis Lam. (grumixama);

Diospyros kaki L. (Persimmon); Garcinia brasiliensis

Mart. (bacupari); Annona muricata L. (graviola); Duguetia

lanceolata A. St.-Hil. (pindaíba); Chrysophyllum cainito

L. (caimito); Anacardium occidentale L. (cashew);

Eriobotrya japonica (Thunb.) Lindl. (medlar) and Litchi chinensis Sonn. (lychee).

The substrate used was composed of a 3: 1:

1 (v/v/v) mixture of soil, sand and bovine manure,

disposed in polyethylene bags (22 x 11 cm). Irrigation was manual, daily, according to substrate moisture

monitoring. Seedlings were kept under a 50% luminosity

cover for a period of 90 days. During the experiment, the minimum temperature was 17 °C and the maximum temperature was 28 °C.

The seedlings selected for this experiment were standardized according to stem height and diameter before inoculation. At the end of 90 days, they were evaluated as to plant height (cm), measuring from the plant base to the apex; stem diameter (mm), in the neck region with the aid of a digital caliper; shoot dry mass (g) and roots dry mass (g) (65 °C, 72 h), as described by Araújo Neto et al. (2015).

Due to the different growth patterns of each fruit species, statistical analysis comparing the results among species was not performed. Thus, for each fruit species, completely randomized design was used in a

factorial scheme 3 (control, sodium alginate and clay) x 2 (presence and absence of microbial inoculum) with

five replications (one repetition), totaling 30 plants.

Data were submitted to analysis of variance (ANOVA)

and means compared by the Tukey test (p≤0.05), using

AgroEstat Software (BARBOSA; MALDONADO JÚNIOR, 2009).

Results and Discussion

Significant effect (P<0.01) of the growth

promoter microorganisms was observed only for C.

cainito L. (caimito) plant height, both for encapsulation in sodium alginate and for microorganisms used in the

inocula (Table 1). For the other species, no significant

differences were observed for plant height, indicating

that the microorganisms did not influence the growth of

seedlings, regardless of type of encapsulation (clay or sodium alginate).

It was reported by Spassin et al. (2016) that

bacterial isolates may have beneficial or no beneficial

effects in relation to the survival and rooting of Eucalyptus

dunnii (Myrtaceae), which raises the hypothesis that the establishment of growth-promoting microorganisms and their association with the plant species may vary according to species, management and, possibly, the place of study. However, Salla et al. (2014) concluded

that the use of PGPB (Streptomyces PM9 rhizobacteria)

resulted in higher yield of indoleacetic acid and a better potential for root induction, as well as in the levels of

phenolic compounds and flavonoids involved in the

defense mechanism of Eucalyptus grandis and E.

globulus plants. The authors also reported alteration in secondary metabolism, suggesting an induced systemic response, indicating their potential use as a biological control in forestry activities.

When analyzing the height variable for the caimito species, it was observed that the encapsulation with clay yielded better results compared to sodium alginate encapsulation, since it did not differ statistically from the control (Table 2). Lower growth of untreated (control) seedlings when compared to growth in the other treatments was also observed (Table 2), suggesting that the use of microorganisms promoted the development of caimito seedlings. Thus, it could be inferred that the associations of bacterial communities associated with the rhizosphere of fruit species are hosts dependent on the taxon, that is, on the species itself, as concluded by Lambais et al. (2014), who studied the rhizosphere of arboreal species of the Atlantic Forest and showed that the bacterial communities associated to trees were

specific to the hosts of plants.

(4)

4

C. H. B. Santos et al.

Rev. Bras. Frutic., Jaboticabal, 2018, v. 40, n. 3: (e-179)

Vaugh (camu-camu) seedlings. For this species, the stem diameter was higher when growth promoting microorganisms were not used, either encapsulated or not (Table 3). This can occur when the microorganisms used present some incompatibility with the native microbiota associated with the plant rhizosphere, which will generate competition between them, altering the positive effects of the target microorganism and, consequently, an unsuitable development of seedlings. Another possible result is due to variable root colonization due to inoculum survival problems or to unfavorable conditions for microorganisms, since the rhizosphere colonization depends on a set of abiotic and biotic factors, including plant genotypes and microorganisms, environmental conditions and the dynamic network of plant interactions

(HARDOIM et al., 2015). However, for C. cainito

(caimito) and L. chinensis (lychee) species, the opposite

occurred, that is, larger stem diameter was observed in both species when seedlings were inoculated with

microorganisms (Table 3). This result confirms the result

observed for plant height variable, in which changes in plant growth may be related to the interaction between microorganisms and rhizosphere.

One possible explanation for this is that soil microorganisms found in the root zone affect plant growth and development, but the potential to take

advantage of these benefits depends on the abundance and diversity of individuals influencing the beneficial

effects on the plant (PANKE-BUISSE et al., 2015). In addition, the same plant species can stimulate diverse microbial communities from one site to another, which provides different responses to the inoculation of a single isolated growth promoter (XU et al., 2016). Additionally, genetic variability in seed propagated seedlings may be considered a factor of plant growth differentiation (HARTMANN et al., 2010).

Lychee seedlings presented significant increases (P<0.05) in the dry mass (DM) content of the plant

shoots with the presence of microorganisms, regardless of whether they were encapsulated or not (Table 4). This result suggests that there may have been an association with the rhizosphere of lychee seedlings, which promoted better establishment of microorganisms and, consequently, provided larger stem diameter, possibly as a function of the higher DM content.

Root dry mass was significantly different only

in caimito seedlings treated with growth promoting microorganisms (Table 5). In this species, root DM accumulation was higher when the substrate was inoculated with microorganisms, regardless of type of encapsulant used.

When evaluating eleven isolates of the genus

Acremonium (GFR6 and GRR1), Colletotrichum

(GFR4 and PFR4), Phomopsis (PFR3 and GCR4),

Cylindrocladium (GRR4), Chaetomium (GRR7) and

Fusarium (GRR5, PRR1 and PRR6), Silva et al. (2006) reported effects of these microorganisms on growth

the parameters of Annona squamosa L. and Annona

muricata L. seedlings with an increase in the shoot

dry matter content of Annona squamosa L. seedlings

between 23.2 and 32.7%, but no isolate affected the root

dry mass content, similar to that observed in this study. Silva et al. (2006) also reported that 20 isolates had a negative effect on the root dry matter content of

Annona squamosa L. seedlings, and observed that in

apparently healthy Annona squamosa L. and Annona

muricata L. tissues, some fungi that could promote the growth of shoots were found, but others could reduce root growth and others that would not affect the growth of seedlings. Another interesting observation is that isolates that promoted the growth of sugar apple seedlings came from graviola, evidencing that isolates from one host can easily colonize hosts of different species, even with greater intensity (Silva et al., 2006). These characteristics

may be associated to the efficiency of root colonization

(5)

5

Promoting fruit seedling growth by encapsulated microor

ganisms

Rev

.

Bras.

Frutic.,

Jaboticabal,

2018,

v.

40,

n.

3:

(e-179)

persimmon (Diospyros kaki) (Ebenaceae); bacupari (Garcinia brasiliensis) (Clusiaceae); graviola (Annona muricata), pindaiba (Duguetia lanceolata) (Annonaceae); caimito (Chrysophyllum cainito) (Sapotaceae); cashew (Anacardium occidentale) (Anacardiaceae); medlar (Eriobotrya japonica) (Rosaceae) and lychee (Litchi chinensis) (Sapindaceae) seedlings 90 days after inoculation with growth promoter microorganisms in two encapsulation methods.

Treatments Jabuticaba Cabeludinha CamucamuGrumixamaPersimmon Bacupari Graviola Pindaíba Caimito Cashew Medlar Lychee

Encapsulation (A) Height (cm)

Control 33.91 a 24.83 a 46.50 a 12.66 a 56.16 a 31.16 a 59.16 a 9.66 a 75.08 a 47.00 a 41.66 a 62.50 a

Clay 34.91 a 24.83 a 38.16 a 11.00 a 59.75 a 41.91 a 58.16 a 8.08 a 77.66 a 43.83 a 40.16 a 44.33 a

Sodium alginate 41.33 a 26.16 a 41.75 a 11.83 a 57.66 a 37.16 a 60.83 a 7.83 a 54.33 b 48.16 a 43.08 a 49.83 a

Inoculum (B) Height (cm)

With inoculum 36.77 a 24.66 a 38.72 a 11.44 a 56.44 a 41.00 a 57.33 a 8.88 a 68.50 a 44.44 a 44.94 a 55.22 a

Without inoculum 36.66 a 25.88 a 45.55 a 12.22 a 59.27 a 42.05 a 61.44 a 8.16 a 69.55 a 48.44 a 38.33 a 52.55 a

CV (%) 22.29 18.57 26.63 21.52 20.19 31.02 15.26 27.67 15.08 15.31 18.88 20.37

F Test

Encapsulation (A) 1.45ns 0.16ns 0.83ns 0.64ns 0.14ns 0.63ns 0.13ns 1.06ns 9.06** 0.60ns 0.21ns 2.77ns

Inoculum (B) 0.00ns 0.30ns 1.67ns 0.42ns 0.26ns 0.02ns 0.93ns 0.42ns 0.05ns 1.28ns 3.18ns 0.27ns

A x B 0.01ns 0.16ns 0.42ns 0.32ns 0.00ns 0.26ns 0.56ns 1.18ns 8.70** 1.17ns 0.79ns 0.05ns

(1)Means followed by the same letter in the column do not differ by the Tukey test, * significant at 5% probability, ** significant at 1% probability and ns not significant.

Table 2. Behavior of height variable of caimito (Chrysophyllum cainito) seedlings (cm) 90 days after inoculation with growth-promoting microorganisms as a function of encapsulation.

Encapsulation (A)

Inoculum (B)

Absence (B1) Presence (B2)

Plant height (cm)

Control (A1) 65.33 aB 84.83 aA

Clay (A2) 74.50 aA 80.83 aA

Sodium alginate (A3) 68.83 aA 39.83 bA

(6)

6

C. H. B. Santos et al.

Rev

. Bras. Frutic., Jaboticabal, 2018, v

. 40, n. 3: (e-179)

Table 3. Stem diameter (DIAM) of jabuticabra (Myrciaria cauliflora), cabeludinha (Myrciaria glazioviana), camu-camu (Myrciaria dubia), grumixama (Eugenia brasiliensis) (Myrtaceae); persimmon (Diospyros kaki) (Ebenaceae); bacupari (Garcinia brasiliensis) (Clusiaceae); graviola (Annona muricata), pindaíba (Duguetia lanceolata) (Annonaceae); caimito (Chrysophyllum cainito) (Sapotaceae); cashew (Anacardium occidentale) (Anacardiaceae); medlar (Eriobotrya japonica) (Rosaceae) and lychee (Litchi chinensis) (Sapindaceae), 90 days after inoculation with growth promoting microorganisms in two encapsulation methods.

Treatments Jabuticaba Cabeludinha Camucamu Grumixama Persimmon Bacupari Graviola Pindaíba Caimito Cashew Medlar Lychee

Encapsulation (A) DIAM (mm)

Control 7.12 a 2.90 a 3.83 a 2.13 a 6.85 a 6.65 a 9.61 a 2.58 a 9.21 a 7.76 a 4.22 a 9.37 a

Clay 7.00 a 2.93 a 3.60 a 2.02 a 5.93 a 6.24 a 8.69 a 2.18 a 9.07 a 6.98 a 3.54 a 8.68 a

Sodium alginate 7.22 a 2.50 a 3.50 a 1.96 a 7.43 a 7.07 a 8.51 a 2.31 a 7.31 a 7.77 a 4.05 a 8.31 a

Inoculum (B) DIAM (mm)

With inoculum 7.14 a 2.84 a 3.32 b 2.07 a 6.77 a 6.31 a 9.00 a 2.37 a 9.27 a 7.24 a 3.92 a 9.64 a

Without inoculum 7. 10 a 2.71 a 3.97 a 2.00 a 6.70 a 6.99 a 8.87 a 2.35 a 7.79 b 7.77 a 3.93 a 7.93 b

CV (%) 11.69 19.19 12.14 17.43 15.23 36.12 10.59 22.49 16.68 14.28 16.32 17.82

F Test

Encapsulation (A) 0.11ns 1.25ns 0.84ns 0.35ns 3.24ns 0.18ns 2.33ns 0.89ns 3.33ns 1.08ns 1.83ns 0.71ns

Inoculum (B) 0.01ns 0.28ns 9.55** 0.19ns 0.02ns 0.36ns 0.08ns 0.00ns 4.89* 1.10ns 0.00ns 5.38*

A x B 2.02ns 0.50ns 0.11ns 0.35ns 1.05ns 0.21ns 2.85ns 0.94ns 0.30ns 0.90ns 0.22ns 0.16ns

(1)Means followed by the same letter in the column do not differ by the Tukey test, being * significant at 5% probability, ** significant at 1% probability and ns not significant.

Table 4. Shoot dry matter (SDM) of jabuticaba (Myrciaria cauliflora), cabeludinha (Myrciaria glazioviana), camu-camu (Myrciaria dubia), grumixama (Eugenia brasiliensis) (Myrtaceae); persimmon (Diospyros kaki) (Ebenaceae); bacupari (Garcinia brasiliensis) (Clusiaceae); graviola (Annona muricata), pindaíba (Duguetia lanceolata) (Annonaceae); caimito (Chrysophyllum cainito) (Sapotaceae); cashew (Anacardium occidentale) (Anacardiaceae); medlar (Eriobotrya japonica) (Rosaceae) and lychee (Litchi chinensis) (Sapindaceae), 90 days after inoculation with growth promoting microorganisms in two encapsulation methods

Treatments Jabuticaba Cabeludinha Camucamu Grumixama Persimmon Bacupari Graviola Pindaíba Caimito Cashew Medlar Lychee

Encapsulation (A) SDM (g)

Control 9.79 a 4.83 a 6.34 a 4.40 a 12.04 a 21.18 a 11.92 a 4.89 a 33.52 a 12.04 a 15.42 a 10.86 a

Clay 9.26 a 5.14 a 4.61 a 4.62 a 11.49 a 18.16 a 12.19 a 4.62 a 34.60 a 11.49 a 12.05 a 11.59 a

Sodium alginate 12.35 a 6.66 a 4.59 a 4.89 a 10.47 a 22.21 a 14.23 a 4.89 a 23.95 a 10.12 a 13.36 a 11.69 a

Inoculum (B) SDM (g)

With Inoculum 10.35 a 5.14 a 4.60 a 4.67 a 11.70 a 16.97 a 11.53 a 4.71 a 35.51 a 11.46 a 14.85 a 12.22 a

Wthout Inoculum 10.58 a 5.95 a 5.76 a 4.60 a 10.97 a 24.97 a 14.04 a 4.89 a 25.88 a 10.97 a 12.38 a 10.54 b

CV (%) 32.50 29.17 31.91 9.46 15.81 75.66 28.17 10.25 40.53 16,17 30.25 13.80

F Test

Encapsulation (A) 1.41ns 0.21ns 2.21ns 1.86ns 1.18ns 0.11ns 0.74ns 0.61ns 1.33ns 1.79ns 1.02ns 0.50ns

Inoculum (B) 0.02ns 1.12ns 2.19ns 0.13ns 0.74ns 0.94ns 2.17ns 0.56ns 2.70ns 0.33ns 1.62ns 5.15*

A x B 0.30ns 0.74ns 0.32ns 0.67ns 0.17ns 0.50ns 3.37ns 1.06ns 0.70ns 0.46ns 1.64ns 0.88ns

(7)

T

able 5

.

Root dry matter (RDM) of jabuticaba

(

Myr

ciaria

cauliflora

), cabeludinha (

Myr

ciaria glazioviana

), camu-camu (

Myr

ciaria dubia

), grumixama (

Eugenia brasiliensis

)

(Myrtaceae); persimmon (

Diospyr

os kaki

) (Ebenaceae); bacupari (

Gar

cinia brasiliensis

) (Clusiaceae); graviola (

Annona muricata

), pindaíba (

Duguetia lanceolata ) (Annonaceae); caimito ( Chrysophyllum cainito ) (Sapotace ae); cashew ( Anacar dium occidentale ) (Anacardiaceae); medlar ( Eriobotrya japonica ) (Rosaceae) and lychee ( Litchi chinensis

) (Sapindaceae), 90 days after inoculation with growth promoting microor

ganisms in two encapsulation methods

T ratamentos Jabuticaba Cabeludinha Camucamu Grumixama Persimmon Bacupari Graviola Pindaíba Caimito Cashew Medlar L ychee Encapsulation (A) RDM (g) Control 6.03 a 1.26 a 2.97 a 1.31 a 5.85 a 7.02 a 8.18 a 1.18 a 10.54 a 1.97 a 3.17 a 3.33 a Clay 5.25 a 1.33 a 2.09 a 1.25 a 5.82 a 5.53 a 6.82 a 1.23 a 1 1.09 a 1.95 a 2.47 a 3.62 a Sodium alginate 7.28 a 1.86 a 1.74 a 1.08 a 5.77 a 6.57 a 5.95 a 1.01 a 6.85 a 2.02 a 2.49 a 3.16 a Inoculum (B) RDM (g) W ith Inoculum 5.97 a 1.44 a 2.01 a 1.25 a 5.91 a 6.07 a 6.98 a 1.1 1 a 1 1.76 a 1.92 a 2.79 a 3.74 a Wthout Inoculum 6.41 a 1.53 a 2.40 a 1.18 a 5.72 a 6.68 a 6.99 a 1.17 a 7.22 b 2.04 a 2.63 a 2.99 a CV (%) 23.26 39.65 32.86 16.24 7.98 68.71 49.33 15.15 43.31 19.80 54.63 26.43 F T est Encapsulation (A) 3.03 ns 1.86 ns 3.26 ns 2.03 ns 0.04 ns 0.18 ns 0.64 ns 2.69 ns 1.89 ns 0.05 ns 0.43 ns 0.40 ns Inoculum (B) 0.42 ns 0.1 1 ns 1.29 ns 0.58 ns 0.78 ns 0.09 ns 0.00 ns 0.64 ns 5.50 * 0.38 ns 0.05 ns 3.17 ns A x B 0.62 ns 0.85 ns 0.33 ns 1.22 ns 0.84 ns 0.21 ns 2.59 ns 0.57 ns 0.47 ns 0.63 ns 1.95 ns 1.01 ns

(1)Means followed by the same letter in the column do not dif

fer by the

Tukey test, being * significant

at 5% probability

, ** significant at 1% probability and ns not significant.

Conclusion

Plant growth promoting microorganisms, regardless of encapsulation used, promote higher development of caimito and lychee seedlings.

Acknowledgements

To the Coordination for the Improvement of Higher Education Personnel (CAPES), by granting a

scholarship to the first author; to Dr. José Carlos Barbosa

for his attention and help in the accomplishment of statistical analyses; to Luiz Carlos de Assis, for assistance in carrying out analyses; and Sidney Bedin, for their assistance in conduction of seedlings. To the São Paulo Research Foundation (FAPESP), for the

research funding number 2014/18313-8

References

ARAUJO NETO, S.E.; FREDNBERG, N.T.N.; MINOSSO, S.C.C., NOVELLI, D. da S.; ANDRADE NETO, R. de C. Substrate conditioners for prodution

of organic cupuasu seedling. Revista Brasileira de

Fruticultura, Jaboticabal, v.37, n.4, 1083-1088, 2015.

(1)

BARBOSA, J.C.; MALDONADO JÚNIOR, W.

Software AgroEstat: sistema de análises estatísticas de ensaios agronômicos. Jaboticabal: Universidade

Estadual Paulista, 2009. (2)

BARRY, A.L.; THORNSBERRY, C. Susceptibility tests: diffusion test procedures. In: BALOWS, A.; HAUSER, W.J.; HERMANN, K.L.; ISENBERG, H.D.;

SHAMODY, H.J. Manual of clinical microbiology.

5thed. Washington: American Society for Microbiology,

1991. p.1117-1125. (2)

BEUTLER, A.N.; BURG, G.M.; DEAK, E.A.;

SCHMIDT, M.R.; GALON, L. Effect of nitrogen-fixing bacteria on grain yield and development of flooded

irrigated rice. Revista Caatinga, Mossoró, v.29, n.1,

p.11-17, 2016. (1)

CARNEIRO, R.M.D.G.; GOMES, C.B. Encapsulação do

fungo Paecilomyces lilacinus em matrizes de

alginato-argila e avaliação da viabilidade dos conídios em duas

temperaturas. Nematologia Brasileira, Piracicaba,

(8)

8

C. H. B. Santos et al.

Rev. Bras. Frutic., Jaboticabal, 2018, v. 40, n. 3: (e-179)

CONSTANSKI, K.C.; ZORZETTI, J.; BOAS, G.T.V.; RICIETO, A.P.S.; FAZION, F.A.P.; BOAS, L.V.; MONNERAT, R.G.; NEVES, P.M.O.J. Seleção e

caracterização molecular de isolados de Bacillus

thuringiensis para o controle de Spodoptera spp. Pesquisa Agropecuária Brasileira, Brasília, DF, v.50, n.8,

p.730-773, 2015. (1)

C O N T R E R A S C O R N E J O , H . A . ; M A C Í A S -RODRÍGUEZ, L.; DEL-VAL, E.; LARSEN, J.Ecological

functions of Trichoderma spp.and their secondary

metabolites in the rhizosphere: interactions with plants.

FEMS Microbiology Ecology, Oxford, v.92, n.4, 2016. 1)

FAHAD, S.; HUSSAIN, S.; BANO, A.; SAUD, S.; HASSAN, S.; SHAN, D.; KHAN, F.; CHEN, Y.; WU, C.; TABASSUM, M.A.; CHUN, M.X.; AFZAL, M.; JAN, A.; JAN, M.T.; HUANG, J. Potential role of phytohormones and plant growth-promoting rhizobacteria in abiotic stresses: consequences for changing environment.

Environmental Science and Pollution Research,

Heidelberg, v.22, n.7, p.4907-4921, 2015. (1)

GÓES, G.S.; GROSS, E.; BRITO-ROCHA, E.; MIELKE,

M.S. Efeitos da inoculação com bactérias diazotróficas e

da adubação nitrogenada no crescimento e na qualidade de

mudas de Inga laurina (SW.) Willd.(Fabaceae). Revista

Árvore, Viçosa, MG, v.39, n.6, p.1031-1038, 2015. (1)

HARDOIM, P.R.; OVERBEEK, L.S.; BERG, G.; PIRTTILÄ, A.M.; COMPANT, S.; CAMPISANO, A.; DÖRIN, M.; SESSITSCH, A. The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes.

Microbiology and Molecular Biology Reviews,

Washington, v.79, n.3, p.293-320, 2015. (1)

HARTMANN, H.T.; KESTER, D.E.; DAVIES, F.T.;

GENEVE, R. Plant propagation:principles and practices.

8th ed. New Jersey: Prentice Hall, 2010. 928 p. (2)

HUNGRIA, M.; NOGUEIRA, M.A.; ARAUJO, R.S.

Soybean seed co-inoculation with Bradyrhizobium spp.

and Azospirillum brasilense: a new biotechnological tool

to improve yield and sustainability. American Journal

of Plant Sciences, Oxford, v.6, n.6, p.811-817, 2015. (1)

LAMBAIS, M.R.; LUCHETA, A.R.; CROWLEY, D.E. Bacterial community assemblages associated with the phyllosphere, dermosphere, andrhizosphere of tree species

of the Atlantic forest are host taxon dependent. Microbial

Ecology, New York, v.68, n.3, p.567–574, 2014. (1)

MAJEED, A; ABBASI, M.K.; HAMEED, S.; IMRAN, A.; RAHIM, N. Isolation and characterization of plant growth-promoting rhizobacteria from wheat rhizosphere

and their effect on plant growth promotion. Frontiers in

Microbiology, Lausanne, v.6, e-198, p.1-10, 2015. (1)

MOTA, M.S.; GOMES, C.B.; SOUZA JÚNIOR, I.T.; MOURA, A.B. Bacterial selection for biological control of plant disease: criterion determination and validation.

Brazilian Journal of Microbiology, São Paulo, v.48, n.1,

p.62-70, 2017. (1)

MÜLLER, T.M.; SANDINI, I.E.; RODRIGUES, J.D.; NOVAKOWISKI, J.H.; BASI, S.; KAMINSKI, T.H. Combination of inoculation methods of Azospirilum brasilense with broadcasting of nitrogen fertilizer

increases corn yield. Ciência Rural, Santa Maria, v.46,

n.2, p.210-215, 2016. (1)

NIETO-JACOBO, M.F.; STEYAERT, J.M.; SALAZAR-BADILLO, F.B.; NGUYEN, D.V.; ROSTÁS, M.; BRAITHWAITE, M.; SOUZA, J.T.; JIMENEZ-BREMONT, J.F.; OHKURA, M.; STEWART, A.; MENDOZA-MENDOZA, A. Environmental growth conditions of

Trichoderma spp.affects indol acetic acid derivatives, volatile organic compounds, and plant growth promotion.

Frontiers in Plant Science, Lausanne, v.8, e-102, p.1-18,

2017. (1)

PANKE-BUISSE, K.; POOLE, A.C.; GOODRICH, J.K.; LEY, R.E.; KAO-KNIFFIN, J. Selection on soil microbiomes reveals reproducible impacts on plant

function. The ISME Journal, London, v.9, n.4, p.980–

989, 2015. (1)

PEREG, L.; DE-BASHAN, L.E.; BASHAN, Y.Assessment

of affinity and specificity of Azospirillum for plants.Plant and soil, Dordrecht, v.399, n.1-2, p.389-414, 2016. (1)

PII, Y.; MIMMO, T.; TOMASI, N.; TERZANO, R.; CESCO, S.; CRECCHIO, C. Microbial interactions in

the rhizosphere: beneficial influences of plant

growth-promoting rhizobacteria on nutrient acquisition process.

A review. Biology and Fertility of Soils, New York, v.51,

n.4, p.403-415, 2015. (1)

SAHM, D.F., WASHINGTON II, J.A. Antibacterial susceptibility tests: dilution methods.In: BALOWS, A.; HAUSER, W.J.; HERMANN, K.L.; ISENBERG, H.D.;

SHAMODY, H.J. Manual of clinical microbiology.

5th ed.Washington: American Society for Microbiology,

(9)

SALLA, T.D.; SILVA, T.R.; ASTARITA, L.V.; SANTARÉM,

E.R. Streptomyces rhizobacteria modulate the secondary

metabolism of Eucalyptus plants. Plant Physiology and

Biochemistry, Paris, v.85, p.14-20, 2014. (1)

SCHOEBITZ, M.; LÓPEZ, M.; ROLDÁN, A. Bioencapsulation of microbial inoculants for better soil–

plant fertilization: a review. Agronomy for Sustainable

Development, Paris, v.33, n.4, p.751-765, 2013. (1)

SHEU, T.Y.; MARSHALL, R.T. Micro-encapsulation of

Lactobacilli in calcium alginate gels. Journal of Food

Science, Hoboken, v.54, n.3, p.557–561, 1993. (1)

SHI, Z.M. Technology for conidial preparation of

Beauveria bassiana. In: LI, Y.W.; LI, Z.Z.; LIANG,

Z.Q.; WU, J.W.; WU, Z.K.; XU, Q.F. (Ed.). Study and

application of entomogenous fungi in China. Beijing:

Academic Periodical Press, 1988. v.1, p.114–115. (2)

SILVA, R.L.de O.; LUZ, J.S.; SILVEIRA, E.B.da;

CAVALCANTE, U.M.T. Fungos endofíticos em Annona

spp: isolamento, caracterização enzimática e promoção do

crescimento em mudas de pinha (Annona squamosa L.).

Acta Botanica Brasilica, Belo Horizonte, v.20, n.3,

p.649-655, 2006. (1)

SOUZA, G.L.O.D.; SILVA, D.F.; NIETSCHE, S.; XAVIER, A.A.; PEREIRA, M.C.T. Endophytic bacteria used as bioinoculants in micropropagated banana seedlings.

Revista Brasileira de Fruticultura, Jaboticabal, v.39,

n.2, e-324, 2017. (1)

SOUZA, R. de; AMBROSINI, A.; PASSAGLIA, L.M.P. Plant growth-promoting bacteria as inoculants

in agricultural soils. Genetics and Molecular Biology,

Ribeirão Preto, v.38, n.4, p.401-419, 2015. (1)

SPASSIN, A.C.; VANDRESEN, P.B.; NEVES, D.; GARCIA, F.A.O.; UKAN, D.PERES, F.S.B. Promoção do

crescimento e enraizamento de miniestacas de Eucalyptus

dunnii por rizobactérias e bactérias do filoplano. Floresta,

Curitiba, v.46, n.3, p.387-395, 2016. (1)

SULTANA, K.; GODWARD, G.; REYNOLDS, N.; ARUMUGASWAMY, R.; PEIRIS, P.; KAILASAPATHY, K. Encapsulation of probiotic bacteria with alginate–starch and evaluation of survival in simulated gastrointestinal

conditions and in yoghurt. International Journal of Food

Microbiology, Amsterdam, v.62, n.1-2, p.47-55, 2000. (1)

VEMMER, M.; PATEL, A.V. Review of encapsulation methods suitable for microbial biological control agents.

Biological Control, San Diego, v.67, n.3, p.380-389,

2013. (1)

XU, S.J.; PARK, D.H.; KIM, J.-Y.; KIM, B.-S. Biological control of gray mold and growth promotion of tomato

using Bacillus spp. isolated from soil. Tropical Plant

Pathology, Brasília, DF, v.41, n.3, p.169-176, 2016. (1)

ZHOU, C.; MA, Z.; ZHU, L.; XIAO, X.; XIE, Y.; ZHU,

J.; WANG, J. Rhizobacterial strain Bacillus megaterium

BOFC15 induces cellular polyamine changes that improve

plant growth and drought resistance. International

Journal of Molecular Sciences, Basel, v.17, n.6, e-976,

Imagem

Table 2. Behavior of height variable of caimito (Chrysophyllum cainito) seedlings (cm) 90 days after inoculation with growth-promoting microorganisms as a function  of encapsulation
Table 4. Shoot dry matter (SDM) of jabuticaba ( Myrciaria cauliflora ), cabeludinha (Myrciaria glazioviana), camu-camu (Myrciaria dubia), grumixama (Eugenia brasiliensis)  (Myrtaceae); persimmon (Diospyros kaki) (Ebenaceae); bacupari (Garcinia brasiliensis
Table 5. Root dry matter (RDM) of jabuticaba (Myrciaria cauliflora), cabeludinha (Myrciaria glazioviana), camu-camu (Myrciaria dubia), grumixama (Eugenia brasiliensis)  (Myrtaceae); persimmon (Diospyros kaki) (Ebenaceae); bacupari (Garcinia brasiliensis) (

Referências

Documentos relacionados

sua mensuração, muitas vezes se tornam difíceis e apresentam grandes falhas de interpretação. No teste do papel a paciente fica em posição supina, que é a posição

A maioria dos ambientes de telefonia IP utiliza por padrão o protocolo RTP para transporte de mídia, sendo o mesmo também atualmente utilizado no ambiente de telefonia IP em

de teoria literária e musical produzidas em Portugal entre os séculos XVII e XIX permitiu-nos efectuar uma análise comparada de procedimentos de Escrita a partir de obras teóricas

O prazo para a confirmação será de 03 (três) dias úteis após a data de vencimento. O candidato que prestar qualquer informação falsa ou inexata, ao se inscrever neste

top-K networks International Conference on Enterprise Information Systems (ICEIS) LIAAD Comunicações em Atas de Conferências Internacionais com Revisores. 2015 Sim Aberto - A

A SUI é composta basicamente por rochas metapelíticas metamorfizadas no fácies anfibolito, cujos resultador foram: quatro variações distintas de xisto (biotita-xisto,

Four traits evaluated show interaction between crosses and structure such as weight of 100 seeds, emergence, emergence speed index and the number of normal seedlings, despite the

Na assertiva de número 01, que os indagou sobre a importância das certificações ambientais das empresas fabricantes de produtos onde compram, discerne-se que 14% dos pesquisados